The seed-borne Southern bean mosaic virus hinders the early events of nodulation and growth in Rhizobium-inoculated Phaseolus vulgaris L.

Abstract

To simulate seed-borne virus transmission, a noninvasive protocol was designed to infect the radicle of germinating seeds, with 100% effectiveness. Preinfection of 24-h-old black bean (Phaseolus vulgaris L.) radicles by Southern bean mosaic virus (SBMV) followed by Rhizobium inoculation 48 h later caused a drastic reduction in root nodulation. Results were attributed to active virus replication within the elongating zone of the radicle at least 32 h before Rhizobium inoculation, which elicited severe anatomical malformations; an abnormal accumulation of apoplastic reactive oxygen species in the rhizodermis, cortex, inner cortical and endodermic root cells; the formation of atypical root hair tips and the collapse of 94% of the root hairs in the SBMV-preinfected radicles. Adult SBMV-preinfected plants showed exacerbated virus symptoms and 80% growth reduction ascribed to major virus-induced ultrastructural alterations in the nodules. The accumulation of ureides, α−amino acids and total reducing sugars in the leaves and nodules of SBMV-preinfected plants are indicators of the hindering effects of SBMV infection on N2 fixation and ureide catabolism, causing N starvation. The exogenous addition of 1 or 4 μM naringenin, genistein or daidzein did not counteract the deleterious effects of SBMV preinfection on nodulation.

Reciprocal plant‐mediated antagonism between a legume plant virus and soil rhizobia

“…Our study provides more evidence that rhizobia can decrease susceptibility to herbivores and pathogens (Dutta et al, 2008;Gopalakrishnan et al, 2015;Mabrouk et al, 2018;Ranjbar Sistani et al, 2017). In contrast, pathogens like PEMV can inhibit plant mutualisms with microbes by suppressing symbiotic genes or interfering with nutrient transfer (Duffy et al, 2003;López et al, 2017). By analysing phytohormone transcripts, we show that interactions between rhizobia, A. pisum, and PEMV were mediated by alterations of hormone signalling.…”

“…At the same time, abiotic and biotic stress above-ground may affect mutualisms between plants and rhizobia. For example, early nodule formation in legumes can be inhibited by pathogens (López et al, 2017;Rao et al, 1987), although herbivory can promote abundance and greater size of nodules (Heath & Lau, 2011;Simonsen & Stinchcombe, 2014). Recent syntheses suggest while herbivores and pathogens alter benefits of microbes for plants, the plant-mediated mechanisms underlying these interactions need further investigation (Friman et al, 2020;Pangesti et al, 2013).…”

Silicon and Nitrate Differentially Modulate the Symbiotic Performances of Healthy and Virus-Infected Bradyrhizobium-nodulated Cowpea (Vigna unguiculata), Yardlong Bean (V. unguiculata subsp. sesquipedalis) and Mung Bean (V. radiata)

“…These differences may account for the enhanced virulence of CMMV in cowpea and yardlong bean, although in mung bean the CCMV and CMMV displayed equal levels of mild virulence. On the other hand, reduced nodulation in virus-infected plants could be the result of virus impairing the early and late events of the symbiosis [ 9 ].…”

“…These three grain legumes have in common the ability to fix atmospheric N 2 via an efficient symbiosis with compatible rhizobial strains belonging mainly to the genus Bradyrhizobium [ 8 ]. Details of the complex processes involving signaling, recognition by both partners and cell division during the early and late events of the symbiosis were recently discussed [ 9 , 10 , 11 ]. In Vigna species, the establishment of the symbiosis is completed with the formation of phaseoloid-type root nodules harboring the rhizobia dedifferentiated into bacteroids and the onset of N 2 fixation.…”

“…As shown by [ 14 ], there is a direct relationship between N availability and the concentrations of AA in different plant organs. In the case of N 2 fixing grain legumes undergoing systemic virus infections, the effectiveness of the symbiosis is severely hampered by the viruses hijacking the plant cellular machinery for replication [ 9 , 15 ].…”